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42Russian Journal of Nematology, 2014, 22 (1), 77-82
Book review
Perry R.N. & Moens M. (eds). 2013. Plant Nematology, Second edition. Wallingford, Oxfordshire, UK and Boston, USA, CABI Publishing, 536 pp. ISBN 978-1-78064-151-5 (hardback); ISBN 978-1-78064-153-9 (paperback)
The second edition of the popular plant nematology book, partially based on lectures of the Postgraduate International Nematology Course, Ghent University, Belgium, is divided into three sections: 1. Taxonomy, Systematics and Principal Genera (chapters 1-6); 2. Biology and Plant-Nematode Interactions (chapters 7-9) and 3. Quantitative Nematology and Management (chapters 10-16), all chapters being written by leading world nematologists. Plant-parasitic nematodes are a major threat to agricultural crops and forestry, influencing the economy and social development of all countries. The efficient control of these pests depends on knowledge of their taxonomic diversity, bionomics, morphology, genetics, population dynamics, associations, host-parasite relationships, and laboratory and field methods. The book is a successful combination of a textbook and detailed reviews of the current achievements in these areas. It is aimed at postgraduate students and researchers in the fields of plant protection, plant quarantine, forestry, agricultural management, zoology and parasitology. The book includes detailed illustrations of excellent quality, and information boxes, which briefly and graphically explain the main definitions and terms. Reading this book is a real pleasure, primarily because of the simple and picturesque English language. The absence of abstracts and summarised conclusions is a drawback, both for each chapter and for the book as whole. Comparing to the first edition of the book, it is clear that all chapter have been revised, especially the chapters on molecular, pest resistance breeding, genetic engineering, biological control and agricultural management, which are completely updated to accommodate the new research information of the 2000s.
Chapter 1, Structure and Classification (Decraemer & Hunt), deals with nematode structures, with a comparative analysis of representatives of the three main phylogenetic lines among nematodes that independently evolved to plant parasitism: tylenchomorphs (mainly using Meloidogyne as an example), triplonchids (Trichodorus) and doryaimids (Longidorus, Xiphinema). The section on comparative ultrastructure and its functional analysis is especially interesting: the apomorphies of the basal cuticle layer are explained by the diverse modes of locomotion in different taxa, and the differences in internal pressure of the hydrostatic skeleton. The change in moulting cuticle is described in sedentary tylenchomorphs. The Nematoda classification is given according to the generally approved system of De Ley & Blaxter (2002) but with some corrections: the family Belonolaimidae is posed as Dolichodoridae Chitwood, 1950, and the family Meloidogynidae is transferred to the Hoplolaimidae at subfamily rank, which does not correspond to molecular data, clustering the root-knot nematodes with Pratylenchus. The neighbouring positions of Aphelenchidae and Aphelenchoididae are retained in the frame of the subfamily Aphelenchoidea, as in the classification of 2002, but this is in contradiction to the newest molecular trees of Holterman et al. (2006). The unity of the family Pratylenchidae is traditionally retained, but in the new multigenic molecular phylogeny this taxon consists of three far-distanced clades. All recent important taxonomic and molecular papers are cited, but the new molecular phylogenetic classification with numerated clades (equivalents of the high taxa) is not incorporated into the classification of 2002.
Chapter 2, Molecular Systematics (Subbotin et al), is based on the most recent publications, and is completely revised. All techniques described in the chapter were used by Subbotin personally; he also was a pioneer in the development of molecular phylogeny models of the taxa used in this chapter as examples to illustrate molecular principles. The species concepts are reviewed, including the asexual species. Methods of molecular systematics are briefly and comprehensively described and illustrated: protein-based techniques, PCR, RFLP, multiplex PCR, RAPD, AFLP, real-time PCR, DNA-hybridization arrays, and the novel isothermal LAMP, which enables identification of nematode species in one reaction tube, suitable for use in field conditions. The taxonomically significant DNA-regions, molecular databases and the programs to process the data, are characterised. Special attention is paid to the ML and Bayesian inference. The molecular trees reconstructions are illustrated using examples of phylogenies of the root-knot nematodes,
cyst-forming nematodes, longidorids, anguinids, pratylenchids and Bursaphelenchus spp. The necessity for using the multigene approach and testing the alternative tree topologies, is emphasised.
In Chapter 3, Root-knot Nematodes (Karssen et al), a review of the pathogenic species is given, with excellent SEM photographs by the authors. The life cycle, invasive juvenile behaviour inside the root during migration through the host tissue, and formation of the polyploid feeding site cells, are thoroughly characterised. The ecology section (including discussion of diapause in relation to the soil parameters) is extremely interesting. It is remarkable, that in the associations of root-knot nematodes with other pathogens, the synergism of Meloidogyne spp. and Fusarium species leads to a break down of the resistance of Fusarium-resistant crops. The techniques of the protein-based and DNA-based species identification, as well as cytogenetics and the different reproduction types, are well described and illustrated. Agricultural management, including the use of trap-cultivation, flooding, solarisation and resistant varieties, biological control with a bacterium Pasteuria and a fungus Purpureocillium, and chemical control with the use of non-fumigant nematicides, is discussed.
Chapter 4, Cyst Nematodes (Turner & Subbotin), includes numerous illustrations by the authors (diagrams, photographs, and schemes). The chapter has the same structure as the root-knot nematode one. Cyst nematodes possess the synapomorphy of a diapausing cyst, to which a mature female is transformed after its death. A cyst contains numerous juveniles, each inside an egg shell. Heteroderids are unique in their narrow host ranges, usually restricted for a cyst nematode species to one plant family. Like root-knot nematodes, cyst nematodes are sedentary endoparasites, their infective juveniles induce feeding sites from the cambial cells near the vascular cylinder of root tip and develop into adults; the feeding site of the mature female consists of the polyploid hypertrophied cells. The illustrated review of the generic diversity with descriptions of species of agricultural importance, is given; the review includes the novel genera, Betulodera, Paradolichodera, Vittatidera. The morphological differences of the potato pests Globodera pallida and G. rostochiensis are distinctly pictured in a diagram. In the section of pathotypes and races, in addition to definitions of terms, examples of virulent genes are given. The spectrum of relationships from synergic to antagonistic relations between cyst nematodes and fungi, Fusarium, Pythium, Rhizoctonia, and the mycorrhizal Glomus, is provided with examples. In addition to the fungi naturally associated with cyst nematodes, there are two commercial biological control agents of cyst nematodes, Nematophthora gynophila and Pochonia chlamydosporium.
In Chapter 5, Migratory Endoparasitic Nematodes (Duncan & Moens), the third nematode taxa in agricultural importance, is reviewed. The chapter is well illustrated with photographs from the laboratories of the authors in 2000s. Identification and morphology, the most important species, life cycles and bionomics, molecular diagnostics, host-parasite relations and associations with other pathogens, and agricultural management of infected crops, are summarised for the group of families: Pratylenchidae (Pratylenchus, Radopholus, Hirschmanniella); Ditylenchus (Anguinidae), Aphelenchoididae (Aphelenchoides spp. and Bursaphelenchus xylophilus). The most prominent feature of the migratory endoparasitic nematodes is the absence of the permanent feeding site and the presence of distinct immune host response; feeding injuries are spread along the migration track through the parenchyma cells, with a trail of dead plant cells and subsequent necrosis following after the nematode in plant roots. The problem of the tropical species group, separated recently from the former widely distributed species P. coffeae, is analysed. The new data on the synergistic relations in the mixed P. brachyurus and Fusarium oxysporum infection on cotton, and the "potato early dying" caused by the synergistic association of Pratylenchus penetrans or P. thornei with fungus Verticillium dahlia, are given. A remarkable symbiosis of the nematode Radopholus similis with the bacteria Wolbachia, earlier known as associated with insects and filarial nematodes, is stated, as well as facultative hermaphroditism of R. similis.
The species of the genus Aphelenchoides (the bud and leaf nematodes A. fragariae and A. ritzemabosi, and the rice nematode A. besseyi) are interesting in their ectoparasitic mode of feeding even inside the host cells within leafs and buds. They have weak stylets and enter the host via the leaf stomata without damaging the epidermis. In their life cycles these nematodes are associated with fungi; they are facultative or obligate mycoparasites. The new data on the aphelenchoidid associations with symbiotic bacteria are given: A. ritzemabosi - Rhodococcus fascians, A. fragariae - Pseudomonas chicorii, Bursaphelenchus xylophilus-Pseudomonas fluorescens.
Chaper 6, Ectoparasitic Nematodes (Decraemer & Geraert), is based on conservative morphological diagnostics, but is also supplied with many new data on ecology and symbiotic relations of the nematodes. The chapter is illustrated with wonderful pictures from CABI editions of previous years. The authors focus
mainly on migratory vectors of viruses: Longidoridae (vectoring nepoviruses) and Trichodoridae (vectoring tobraviruses). The virus-vector nematodes are the fourth most important nematode group according to the damage they cause to the agricultural crops. The detailed review of the Longidorus and Xiphinema species groups includes morphology, associations with viruses, host plant ranges, distribution and the nematode-caused diseases, life cycles with the thermal optima for species, and vertical migration. The species of the family Trichodoridae, especially the most important for temperate regions (Trichodorus similis and Paratrichodorus pachydermus), and the tropics (Nanidorus minor), are thoroughly characterised. The most interesting data on virus vector nematodes are their relations with viruses: nepoviruses are localised at the inner surface of the odontostyle and its guiding sheath (Longidorus), and of the odontophore (Xiphinema), while the tobraviruses are spread along the pharyngeal duct (Trichodorus), outside the onchiostyle. Only the specific virus serotypes attach at the cuticular canal surface of the corresponding vector nematode. Tobraviruses of virus vector nematodes are used in genetic engineering to silence of the specific plant resistance genes.
In Chapter 7, Reproduction, Physiology and Biochemistry (Perry et al), the processes of sex determination types (X0, XY, the physiologically stimulated one in root-knot nematodes) reproduction (amphimixis, meiotic and mitotic parthenogenesis, pseudogamy, hermaphroditism, and moulting, is clearly reviewed. In the biosynthesis section there are new data on lipid metabolism, because the lipid compounds are the most important energy reserves in plant-parasitic nematodes, in relation to their predominantly aerobic respiration, low temperatures of their habitats, and the presence of dormant stages in their life cycles. Among lipid compounds the most important are the glycolipids and sterols, which act as modulators of cell membrane fluidity and as precursors of biologically active molecules, such as steroid hormones; among carbohydrates chitin, which is a polymer of N-acetylglucosamine, is the most significant, as a major component of nematode eggshells. The main features of respiration, catabolism of main compound classes, and osmoregulation, are reviewed. The most interesting part in the chapter is the section on survival strategies. Of the dormant stages, the authors differentiate diapause (the obligatory part of the life cycle, entrance and exit from which is regulated by special combination of pheromones and external signals), quiescence (as cryobiosis and anhydrobiosis, with the simple dormant stages reversible when favourable external conditions return), and dauers, which are the alternative dormant life cycle stages for surviving unfavourable conditions for long periods. The survival strategies are described for different nematode taxa with a special attention to anhydrobiosis causing the changes in behaviour: body coiling, clumping (or aggregation); in the cell structures of mitochondria and lipid granules; in the metabolic processes: carbohydrates and lipids transform into trehalose and glycerol to protect proteins from autolysis. The hatching biology including signals, root diffusates, alteration of eggshell membranes, are discussed for different taxa.
Chapter 8, Behaviour and Sensory Perception (Perry & Curtis), is one of the best reviews to be read to understand the nematode style of life; this chapter has been completely revised using the most recent publications. The authors analyse the physiology and ultrastructure of both chemosensilla (amphids, phasmids, male supplements) and mechanosensilla and their use in different behaviour types. The neuromuscular structure, neurons, their nets and links with muscle cells, sensory and impulse transduction, are described in depth. The detailed vector analysis of the nematode undulatory propulsion and the mathematical basis (Reynolds' index of 0.01) for such type of movement in a viscous medium such as water, is given. It is proved that an undulatory amplitude and a rate of propulsion depend only on the water matric potential (i.e. of surface tension and thickness of a film of water) and both movement parameters are independent of the size of soil pores and the ratio of clay to sand particles. Two-dimensional sliding, on a surface of three-dimensional mosaic of the water film lenses, serves as an efficient adaptation to overcome hindrances, which is limited only by the total surface of a film but not by the water volume in pores. Among responses to stimuli the authors differentiate taxis (orientation) and kinesis (acceleration, frequency increase); e.g., the temperature increase gradient of 0.01 cm-1 is sufficient for accelerated migration; movement of Meloidogyne is up, whereas movement of Rotylenchulus is down and foliar parasites move towards cool regions. Authors separate the stimuli to three groups: long distance, short distance and local attractants (or repellents). For example, the gradient of the dissolved CO2 is a long distance attractant, whereas the gradients of ammonium nitrates and root diffusates are local repellent and local attractant, respectively. The behaviour is analysed separately for the ectoparasitic, migratory endoparasitic and sedentary endoparasitic nematodes, during infection, migration in the host tissues, and feeding. The infective juveniles (J2) of cyst nematodes migrate in host tissues intracellularly thus damaging plant cells, whereas J2
of Meloidogyne migrate intercellulary causing much less damage and necrotic reactions. In both groups the change of the J2 pharyngeal gland secretion activities takes place: in the early stages of parasitism activity of the subventral glands increased during invasion and during feeding site induction; products of the dorsal gland cell primarily play a role later in the feeding site development near the root vascular cylinder. The stem nematode Ditylenchus phyllobius penetrates the epidermis only in the embryonic leaf folds in buds, whereas Aphelenchoides spp. penetrate the leaf via stomata using the gradient CO2 as the orientation attractant.
In Chapter 9, Gheysen & Jones describe the Molecular Aspects of Plant-Nematode Interactions. The most important event in plant parasitism is the mechanical and enzymatic destruction of the cell walls framed with the crosslinked cellulose microfibrils. The nematode cellulases have been acquired by horizontal gene transfer from bacteria in root-knot nematodes, and from fungi in Bursaphelenchus xylophilus. The reconstruction of the cell mitotic cycle takes place in the multinucleate feeding sites: in the root-knot nematodes' sites the M-phase activation without cytokinesis influenced by the plant hormone zeatin, whereas in the cyst nematodes' feeding sites the S-phase without nucleic mitoses leads to the DNA endoreplication influenced by the ubiquitin protein promoter. The promoters of auxin and the genes induced by auxin are activated in the mitotic cycle transformation.
Plant immune reactions have similar features with the immune responses in animals: in both processes free oxidative radicals and the effector-induced pathways with lipid-bound molecules are involved. Nematodes use the mimic protection of their hypodermic and surface coat proteins, as well as the pharyngeal gland and excretory system secretions, to interrupt the plant defence reaction (the jasmonate pathway).
The basic plant defence models are described: the Guard Hypotheses and the Zigzag model of Jones and Dangl. The latter postulates the presence of three levels of protection: i) the level of the cell surface pattern recognition receptors, which detect the conservative pathogen markers and activate pattern-triggered immunity (PTI); ii) a second layer of immune receptors to detect the presence of effectors, leading to effector-triggered immunity (ETI); and iii) the hypersensitive response (HR). To overcome these barriers, the nematode interrupts the salicylic acid resistance pathway (with chorismate mutase) and the intracellular protein kinase signalling pathways (with the nematode protein, which is a functional analogue of the plant peptide).
The Chapters 10, Plant Growth and Population Dynamics, and 11, Distribution Patterns and Sampling, (Been & Schomaker) are devoted to the problems of population dynamics, yield loss modelling and nematode distribution. The distribution of nematodes reflects the history of agricultural management and the presence of resources, especially the plant hosts.
In practice, it is necessary to define appropriate sampling pattern, number of cores, and what size of sample is required. These parameters are different for the following purposes: i) to determine the presence or absence of a certain nematode species; ii) to estimate population densities of the target nematode in small plots; and iii) to estimate population densities in a farmer's field of a certain size, and to do the yield loss prognosis.
The distribution of nematodes is usually aggregated; therefore, the negative binomial distribution (NBD) is assumed in most cases. The NBD equations are used where the grade of aggregation is expressed as K. To simplify the field research, the soil sample size of 1.5 kg 1 m-2 plot is accepted and the tables of K-values are developed for different nematode species, where the dimensions and number of sampling plots, number of cores per plot are given. To decrease the CV value to the required level (usually 15% for the yield loss prognosis, but it depends on the number of extracted nematodes), it is recommended to use smaller cores but increase their number in a plot bulk sample.
Mapping of the infestation hotspots is important for pest management. Hotspots (foci) are stretched along planting rows. In the centre of infestation hotspot the nematode population density may be decreased because of death of plants; but the density grows exponentially from the periphery to the centre, reaching the host maximum carrying capacity. To detect the infestation hotspots reliably with a minimum number of samples (the area of the field, divided by the mean area of the infestation focus), the distance between the nodes of rectangular grid has to be not more than focus size, taking into account the length/width ratio of the hotspot. The size of a hotspot may be estimated visually at the beginning.
The vertical distribution is an important factor influencing sampling. It depends on the depth of the roots of the target crops, and on soil drying in the upper 3 cm. In the majority of species, 90% of specimens are concentrated in the upper 35 cm of soil. As a standard depth of sampling, the bulk sample of 0-25 cm soil profile for tylenchs (a ploughing layer with uniform nematode densities), and the 0-50 cm layer for longidorids and trichodorids, is accepted.
Chapter 12, International Plant Health - Putting Legislation into Practice (Hockland et al), is devoted to the acts and initiatives of the phytosanitary legislations and the technology tools to estimate the risks from plant-parasitic nematodes. The chapter includes information on certification procedures, eradication programmes for Radopholus (in tropical crops) and Globodera (potatoes), and poses the newest challenges that are associated with the growing controversy between the quarantine pests' lists and directives and the newly described molecularly based species and pathotypes of nematodes.
Chapter 13, Biological and Cultural Management (Viaene et al), starts with the delimitation of the definitions of nematode management as a system of measures to achieve the manipulation of nematode densities to non-injurious or sub-economic threshold levels, and nematode control which implies the use of a single measure to reduce or eliminate nematodes. Further delimitation separates cultural management, as the system to use microbiological technology and organic materials, from biological management, which is a suppression of plant diseases and pests with the aid of living antagonistic organisms. Biological management should be considered within the framework of other management strategies, especially with cultural control methods. The use of the trap cropping, nematode antagonistic plants such as Tagetes spp. and Asparagus officinalis, cover crops, a shift of planting time to avoid periods of peak activity of nematode invasive stages and thus to reduce nematode damage (planting at sub-optimal temperatures), are highly efficient as parts of a management system. The functional principles of suppressive soils and green manures are described.
Only a few fungi species have been successful in field trials as biological control agents for cyst nematodes, root-knot nematodes, Radopholus similis and Tylenchulus semipenetrans. Some are now introduced in practice as commercialised strains; they are Purpureocillium (syn. Paecilomyces) lilacinus-251 and the fungus Pochonia chlamydosporia, with different lines against cyst and root-knot nematodes combining with poor hosts to reduce the infestation before the next susceptible crop. The fungus Trichoderma spp. to control M. javanica is used in combination of two lines T. asperellum-203 and T. atroviride IMI 206040 to increase control level. The control action is based on the proteases and chitinolytic enzyme activities. Among the endophytic fungi, the mycorrhizal Glomus spp. are effective agents against Meloidogyne spp.
Bacteria are important antagonists of nematodes (Burkholderia spp., Pseudomonas spp., Bacillus spp.) because of their antibiotics and toxins; they also induce the plant growth and resistance. The highly specific parasitic endospore-forming bacteria Pasteuria spp. have been developed for a long time as biological control agents against nematodes; now the mass culturing commercial technology has been developed by Pasteuria Bioscience Inc., now part of Syngenta. After selection of the natural source of the aggressive biological agent strain, it is necessary to develop the technology for its mass culturing in artificial media, formulation for storage, transportation and the application modes (the bare-root dips or an input in soil, frequency of application and dosage).
Chapters 14 and 15, Nematode Resistance in Crops (Starr et al) and Genetic Engineering for Resistance (Cottage & Urwin) are similar to chapter 9 in principles. The genetic engineering is aimed at cultural management without pesticides and with a minimum of ecological risks. The main task is to identify the qualitative trait loci (QTL) conferring nematode long-term and broad resistance, using the modern technology of the genetic polymorphism screening. The earlier Gene-for-Gene hypothesis of Harold Flor is now substituted by the Guard Hypothesis of Dangl and Jones; according to the latter, the pathogen Avr-gene product binds to a target (effector), which in uninfected cells binds to the R protein, a product of the R-gene monitoring system of plant's defence. As a result, upon binding of the Avr product to the target, the R protein becomes unbound and active and initiates the plant's defence pathways. Genetic engineering uses different approaches: the gene copy number variation (soybean gene rhg1), the disruption of the synthesis of nematode enzymes pathways, which are important for the feeding site induction of sedentary parasites (rhg4, a-SNAP, WI12), and the involvement of the resistance genes already used against fungi, viruses and insects (RAR1, HSP90). In many cases the transgenic resistance does not lead to the cell death caused by the local hypersensitive plant reaction, but only suppress the establishment of feeding sites, or block the chemoreceptors (amphids) of the infective juveniles with plantbodies and lectins.
The most successful in field trials and agricultural practice is of the use of transgenic plants with the cysteine and serine proteinase inhibitors to control M. incognita (on the rice crops), Radopholus similis (bananas), G. pallida (potatoes), H. glycines (soybeans) and Pratylenchus penetrans (alfalfa); these inhibited proteinases are digestive intestinal enzymes of the nematode.
In the genetic engineering technology the most important chain link is a promoter molecule, which is the highly nematode species-specific trigger of the defence pathways of the plant cell death system. For
successful plant protection, genetic engineering has to stack several resistances to the pathogen in the plant, preferably targeting different aspects of the nematode's life cycle and to utilise the engineered resistances as part of a panel of methods that can be used in integrated pest management that may include pesticides, natural resistances, crop rotation, trap cropping and biocontrol measures, because the single resistance generates a strong selective pressure to facilitate the increase of alternative nematode pest species (M arenaria instead ofM. incognita, G. pallida instead of G.rostochiensis).
Chapter 16, Chemical Control of Nematodes (Haydock et al) is focused not only on the modern nematicides diversity and application practice, but also includes information about bionematicides and the analysis of the influence of the pesticides for environment, human health and safety.
Alexander Yu. Ryss, Zoological Institute RAS, St. Petersburg
